Concentrations of organochlorine pesticides and polychlorinated biphenyls in human serum and adipose tissue from Bolivia

Environmental Research 112 (2012) 40–47

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Concentrations of organochlorine pesticides and polychlorinated biphenyls in human serum and adipose tissue from Bolivia$ J.P. Arrebola a,n, M. Cuellar b, E. Claure b, M. Quevedo b, S.R. Antelo b, E. Mutch c, E. Ramirez b, M.F. Fernandez a,d, N. Olea a,d, L.A. Mercado b a

Laboratory of Medical Investigations, San Cecilio University Hospital, University of Granada, 18071 Granada, Spain ´noma Gabriel Rene´ Moreno, Instituto de Investigaciones en Ciencias de la Salud, Carreras de Bioquı´mica y Farmacia, Universidad Auto ´xico s/n, Santa Cruz de la Sierra, Bolivia Calle Me c Institute of Cellular Medicine, Newcastle University. Newcastle upon Tyne, NE2 4HH, UK d ´ blica (CIBERESP), Spain CIBER en Epidemiologı´a y Salud Pu b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 7 June 2011 Received in revised form 13 September 2011 Accepted 14 October 2011 Available online 9 November 2011

Organochlorine pesticides and polychlorinated biphenyls (PCBs) are synthetic chemicals that are highly resistant to biodegradation and have proven adverse health effects. The objectives of this study were to determine concentrations of three selected organochlorine pesticides (p,p0 -DDT, p,p0 -DDE, HCB) and three specific PCB congeners (PCB 138, 153, 180) in adipose tissue and serum samples from an urban adult population (n ¼ 112) in the city of Santa Cruz de la Sierra, Bolivia, and to investigate their relationships within and between the two matrices and with selected socio-demographic characteristics. The percentages of samples positive for these compounds ranged from 40% for PCB 180 to 100% for p,p0 -DDE in adipose tissue, and from 21% for HCB to 93% for p,p0 -DDE in serum. Median number of residues per sample was five for adipose tissue and three for serum. Geometric mean concentrations indicate a considerable historical and recent exposure to organochlorine pesticides and PCBs in this population. Adipose tissue:serum ratios ranged from 149.3 to 590.3 (wet basis) and from 0.9 to 3.5 (lipid basis). We found positive and statistically significant correlations between adipose tissue and serum concentrations only in p,p0 -DDE and HCB. This novel study in Bolivia underlines the need for human biomonitoring to assess exposure to environmental pollutants in South America. & 2011 Elsevier Inc. All rights reserved.

Keywords: Persistent organic pollutant Organochlorine pesticide Polychlorinated biphenyl Serum Adipose tissue

1. Introduction Persistent organic pollutants, such as organochlorine pesticides and polychlorinated biphenyls (PCBs), are synthetic chemicals that are highly resistant to biodegradation. Due to their persistence and lipophilicity, persistent organic pollutants tend to bioaccumulate and biomagnify in the food chain, resulting in the considerable

Abbreviations: PCBs, polychlorinated biphenyls; DDT, dichlorodiphenyltrichloroethane; DDE, dichlorodiphenyldichloroethylene; HCB, hexachlorobenzene; BMI, body mass index $ Funding and ethical approvals: The study was partially supported by the ‘‘Impuesto Directo a Hidrocarburos’’ (IDH) of the Government of Bolivia. During the field work and chemical analyses, Dr. J.P. Arrebola was a research fellow from ˜ ola de Cooperathe Spanish Agency for International Cooperation (Agencia Espan cio´n Internacional; MUTIS III-B program). The funding agencies had no role in the analysis of data or preparing the manuscript. This research was approved by the Ethics Committee of the Human Health Sciences Faculty (Comisio´n de E´tica e Investigacio´n de la Facultad de Ciencias de la Salud Humana), Universidad Auto´noma Gabriel Rene´ Moreno. n Corresponding author. Fax: þ34 958 249953. E-mail address: [email protected] (J.P. Arrebola). 0013-9351/$ - see front matter & 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.envres.2011.10.006

exposure of living organisms (Porta et al., 2008; Rollin et al., 2009). Furthermore, persistent organic pollutants can be transported over long distances in the atmosphere and therefore be distributed to regions in which they have never been used (UNEP, 2002). Persistent organic pollutants are contaminants in air, water, soil, and plants, among other environmental media (Ritter et al., 1996). Organochlorine pesticides have long been widely used in agriculture and in public health as highly effective pest control agents (UNEP, 1999). Thus, the insecticide dichlorodiphenyltrichloroethane (DDT) has been used extensively worldwide in agriculture and for vector control since 1939 (Turusov et al., 2002). Technical grade DDT consists of a mixture of several compounds, including the isomers o,p0 -DDT and p,p0 -DDT. Once in the environment or living organisms, DDT is mainly metabolized to p,p0 -dichlorodiphenyldichloroethylene (p,p0 -DDE), which is even more persistent than its parent compound (UNEP, 1999). Both p,p0 -DDT and p,p0 -DDE have been proven to be estrogen receptor agonists and androgen receptor antagonists (Li et al., 2008), and DDT is considered a possible human carcinogen by the International Agency for Research on Cancer (UNEP, 2002). In Bolivia, an estimated 1.5 t of organochlorine pesticides remained

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stored in controlled disposal sites in 2004 (Ministerio de Desarrollo Sostenible, 2004). Hexachlorobenzene (HCB) was first introduced in 1945 as a fungicide to treat onions, sorghum, and similar crops. Other sources of HCB include by-product emissions of the chemical industry, impurities in organochlorine pesticide mixtures, combustion reactions, wood preservation agents, and metallurgical processes (Barber et al., 2005). HCB is known to affect the human liver, causing porphyria cutanea tarda, and it has also been classified as a possible human carcinogen by the International Agency for Research on Cancer (UNEP, 2002). In vitro studies have found HCB to be an androgen receptor antagonist (Li et al., 2008). To the best of our knowledge, no information is available on HCB uses or disposal in Bolivia. PCBs, manufactured since 1929, have been used worldwide in numerous industrial and commercial applications, including transformer and capacitor oils, hydraulic and heat exchange fluids, and lubricating and cutting oils (La Rocca and Mantovani, 2006). PCBs have been classified as probable carcinogens by the International Agency for Research on Cancer and, depending on the spatial orientation of their chlorine constituents, some congeners exhibit weak estrogenic activity, whereas others act as antiestrogens (ATSDR, 2000). It has been reported that 17,200 l of dielectric fluids potentially contaminated with PCBs remained stored in 2004 in electric and mining companies in Bolivia (Ministerio de Desarrollo Sostenible, 2004). Since the early 1970s, most countries have banned or severely restricted the production, handling, and disposal of persistent organic pollutants, due to their high persistence in the environment and their proven or suspected clinical effects at doses traditionally considered safe, including reproductive disorders, teratogenicity, endocrine disruption, and carcinogenicity (Olea et al., 2001a, 2001b; Porta et al., 2008; UNEP, 2002). Nevertheless, it has been reported that persistent organic pollutants are still used in several countries, either legally (e.g., in vector control campaigns) or illegally (Porta et al., 2008; Roberts et al., 1997; UNEP, 2002). Exposure to environmental pollutants is of particular concern in the populations of developing countries, because of inadequate legislation on this matter, the increasing presence of manufacturers, and the lack of trained personnel and equipment (el Sebae, 1993). In South American countries, the lack of regular scientific biomonitoring studies means that scant data are available on human exposure to persistent organic pollutants, and several populations might be especially at risk (UNEP, 2002). Adipose tissue offers a good measure of cumulative internal exposure to persistent organic pollutants, accounting for all routes and sources of exposure (Kohlmeier and Kohlmeier, 1995; Pearce et al., 1995). Lipid-adjusted values provide a more accurate picture of the total burden of these residues in adipose tissue throughout the body (Patterson et al., 1988). Serum levels of persistent organic pollutants reflect the recirculation of xenobiotics released from adipose tissue due to lipolysis and current exposures (Crinnion, 2009). The objectives of this study were to determine concentrations of three selected organochlorine pesticides (p,p0 -DDT, p,p0 -DDE, HCB) and three specific PCB congeners (PCB 138, 153, 180) in adipose tissue and serum samples from an adult population in the city of Santa Cruz de la Sierra, Bolivia, and to investigate their relationships within and between the two matrices and with selected socio-demographic characteristics. 2. Materials and methods 2.1. Study area Santa Cruz de la Sierra, the city with the largest population in Bolivia (1,500,000 inhabitants), is located in the eastern part of the country (Santa Cruz Region) at an altitude of 416 m a.s.l. (Fig. 1). The economy of the city and its

41

Fig. 1. Study area. Extracted and modified from: http://www.wikipedia.org/.

suburbs represents 35% of the Gross Domestic Product of Bolivia and is based on the hydrocarbon industry, logging, and agriculture. Around 80% of the total agricultural product of the country is grown in this tropical region, with an average annual temperature of 21 1C. 2.2. Design and population Between January and June 2010, study participants were randomly recruited from individuals undergoing non-cancer-related surgery (56% inguinal hernia or abdominal surgery; 20% gall bladder surgery, and 24% other surgeries) at the Hospital Japone´s in Santa Cruz de la Sierra. The surgical treatments allowed adipose tissue and blood samples to be obtained in an ethical and practically feasible manner. Inclusion criteria were: age above 16 years, absence of hormonerelated disease or cancer, no hormone therapy, and residence in the study area for at least 10 years. Out of 160 individuals meeting these criteria and invited to take part, 112 (69%) signed their informed consent to participate in the study, which was approved by the ethics committee of the hospital. 2.3. Independent variables Information on possible predictors of persistent organic pollutants exposure was derived from an ad hoc questionnaire completed by each participant before surgery and conducted face-to-face by trained interviewers during the hospital stay. Socio-demographic characteristics included information on sex, age, body mass index (BMI), residence, occupation, diet, and smoking habit. Participants0 height and weight were measured and the BMI was calculated as weight/height squared (kg/m2). Subjects were classified into six occupational categories following Goldthorpe’s proposal (Regidor, 2001; Domingo-Salvany et al., 2000): I, managers of companies with Z10 employees, senior technical staff, and free professionals; II, managers of companies with less than 10 employees and intermediate occupations; III, administrative personnel, financial management support professionals, self-employed professionals, supervisors of manual workers, and other skilled non-manual workers; IV, skilled and semi-skilled manual workers; and V, unskilled manual workers. Because of sample size limitations, we classified subjects into 2 groups (non-manual workers: I þII þIII; manual workers: IVþ V). In smokers, data were gathered on the number of cigarettes consumed per week and it was included as an interval variable. The residence was considered ‘‘urban’’ when within the city of Santa Cruz de la Sierra at the time of the surgery and ‘‘rural’’ when in any town/village surrounding the city. 2.4. Sampling and chemical analysis Samples of adipose tissue (5–10 g) and blood (10 mL) were collected during surgery and immediately coded and stored at  80 1C until chemical analysis. The main sources of adipose tissue were pelvic waist (56%) and front abdominal wall (44%). The chemical extraction procedure to isolate analytes from adipose tissue and serum samples has been reported elsewhere (Martinez Vidal et al., 2002; MorenoFrias et al., 2004). Briefly, 200 mg of adipose tissue was extracted using n-hexane, and the solution was then purified through 200 mg alumina in a glass column and kept in test tubes at  80 1C. From each serum sample, 4 mL was extracted with acidified diethyl ether and n-hexane, and the cleaned-up extract was eluted through a solid phase silica extraction column (Sep Pack, Waters). Organochlorine pesticides (p,p0 -DDT, p,p0 -DDE, and HCB) and PCBs (congeners 138, 153, and 180) were quantified by high-resolution gas chromatography with

42

J.P. Arrebola et al. / Environmental Research 112 (2012) 40–47

micro-electron capture detection, using an Agilent GC7890A system (Agilent Technologies, Wilmington, DE) and a 30 m  0.32  0.25 mm silica capillary column; p,p0 -dichlorobenzophenone was used as the internal standard. Limits of detection were considered the smallest amount of analyte giving a signal-to-noise ratio Z3 and were set at 1 ppb for each analyte. Organochlorine pesticide and PCB concentrations were confirmed in one out of every ten analyzed samples by means of gas chromatography coupled mass spectrometry, using a 6890 Agilent (Agilent Technologies) gas chromatograph with a 7683 series injector and quadruple mass selective detector. Total lipid content was quantified gravimetrically in adipose tissue using a previously reported method (Rivas et al., 2001), dissolving 200 mg of adipose tissue homogenate in 5 mL of chloroform:methanol:hydrochloric acid (20:10:0.1, v/v/v). After repeating the process, 10 mL of 0.1 N HCl was added and centrifuged at 3000 rpm for 10 min. The organic phase was then collected. After drying under a nitrogen stream, extracts were weighed, expressing the total lipid in grams of lipid per gram of adipose tissue. For serum samples, lipid content was calculated as described by Phillips et al. (1989). Persistent organic pollutant concentrations were expressed both as nanograms per gram of adipose tissue/nanograms per mL (wet basis) and as nanograms per gram of lipids (lipid basis). A double-blinded procedure was followed, with none of the chemical analysts or statisticians being aware of the identity or characteristics of any study subject. The reproducibility and extraction efficacy of the method were established by running 10 adipose tissue and serum samples spiked with the target analytes at an intermediate point on the calibration curve. The samples were processed as described above. Recoveries ranged from 70% to 98%. 2.5. Statistical analysis Both wet- and lipid-basis adipose tissue:serum ratios were calculated by dividing each adipose tissue concentration by each serum concentration. Concentrations below the limit of detection were assigned a random value between zero and the limit of detection. Because the distribution of persistent organic pollutants concentrations was non-normal, results were log-transformed and geometric means and geometric standard deviations were calculated. Bivariate analyses were carried out using the Mann–Whitney U-test and Spearman’s correlation test. The significance level was set at p ¼ 0.05 and p-values below 0.10 were considered to be borderline significant. All tests were two-tailed. SPSS v18.0 (SPSS, Chicago, IL, USA) was used for the data analyses.

3. Results 3.1. Socio-demographic characteristics A description of the main characteristics of the study population is shown in Table 1. There was a higher proportion of females (n¼90, 80.4%) than males (n ¼22, 19.6%) in comparison to official

surveys in the study area (51% males, 49% females (INE, 2010). The mean age of the study population was 31.4 years, slightly lower than the 33.9 years reported in a census of Santa Cruz de la Sierra residents (age 18–70 years, INE, 2010). The majority of subjects were overweight according to the World Health Organization classification (WHO, 2010). There were no statistically significant differences in sex and age between study participants and non-participants (data not shown). 3.2. Occurrence of persistent organic pollutants Frequencies and concentrations of organochlorine pesticides and PCBs in serum and adipose tissue samples are shown in Table 2. All analyzed samples were positive for one or more persistent organic pollutant residues. A median of five residues was detected in adipose tissue samples and three in serum samples. The frequencies of persistent organic pollutant residues detection ( Z limit of detection) ranged from 100% for p,p0 -DDE to 40% for PCB congener 180 in adipose tissue and from 93% for p,p0 -DDE to 21% for HCB in serum samples. p,p0 -DDE showed the highest geometric mean adipose tissue concentration (386.6 ng/g lipid) and highest serum concentration (267.4 ng/g lipid). Table 3 exhibits the geometric mean of ratios between adipose tissue and serum concentrations, using both wet and lipidadjusted values. Wet-basis ratios ranged from 149.3 to 590.3, while lipid-weight basis ratios ranged from 1 to 2, with the exception of PCB 138 (ratio¼3.6) and PCB 153 (ratio¼ 0.9). Table 4 shows the Spearman correlations among concentrations of the studied persistent organic pollutants in serum and in adipose tissue and the correlations between adipose tissue and serum concentrations of each chemical. Serum concentrations of most persistent organic pollutants were positively correlated except for PCB 153, which showed a statistically significant negative correlation with HCB. In general, adipose tissue concentrations showed similar positive correlations, except that p,p0 -DDT was negatively correlated with HCB. The correlation between p,p0 DDT and p,p0 -DDE in adipose tissue (Spearman correlation¼0.2, po0.010) was not observed in serum. A significant correlation between serum and adipose tissue concentrations was found only for p,p0 -DDE (Spearman coefficient¼0.3, po0.05) and HCB (Spearman coefficient¼0.2, po0.10).

Table 1 Characteristics of the study population (n¼112). n (%)

Mean (standard deviation)

Median

Range

Age (yr)

112 (100)

31.4 (12.6)

28.0

18.0–70.0

Sex Male Female

22 (20) 90 (80) 26.6 (3.5)

26.4

17.8–35.4

80 (71) 32 (22) 111 (99)

145.3 (104.7)

144.0

2.0–480.0

23 4 23 61 11 110

0.8 (4.1)

0.0

0.0–35.0

BMI (kg/m2) Underweight (o 18.5) Normal (18.5–25) Overweight (25–30) Obese ( 430) Residence Urban Rural Time of residence (months) Occupational categories I þII (non-manual) III (non-manual) IV þV (manual) Homemaker (manual) Smoker No. cigs/week

112 0 31 62 19

(100) (0) (28) (55) (17)

(21) (4) (21) (55) (10) (98)

J.P. Arrebola et al. / Environmental Research 112 (2012) 40–47

43

Table 2 Concentrations of selected persistent organic pollutants in serum and adipose tissue. % above limit of detection

Geometric mean

Geometric standard deviation

Percentiles 25th

Serum HCB p,p0 -DDE p,p0 -DDT PCB 138 PCB 153 PCB 180 Adipose tissue HCB p,p0 -DDE p,p0 -DDT PCB 138 PCB 153 PCB 180

ng/mL ng/g lipid ng/mL ng/g lipid ng/mL ng/g lipid ng/mL ng/g lipid ng/mL ng/g lipid ng/mL ng/g lipid

21

0.1 22.1 1.2 267.4 0.1 13.0 0.2 33.7 0.3 59.0 0.1 26.7

93 50 56 80 38

ng/g ng/g lipid ng/g ng/g lipid ng/g ng/g lipid ng/g ng/g lipid ng/g ng/g lipid ng/g ng/g lipid

82

21.1 26.3 309.3 386.6 32.3 40.31 84.0 105.0 52.7 65.8 32.8 41.0

100 73 87 81 40

Table 3 Adipose tissue:serum ratio of each persistent organic pollutant.

HCB p,p0 -DDE p,p0 -DDT PCB-138 PCB-153 PCB-180

Wet basis Lipid basis Wet basis Lipid basis Wet basis Lipid basis Wet basis Lipid basis Wet basis Lipid basis Wet basis Lipid basis

Geometric mean

Geometric standard deviation

310.3 1.86 299.3 1.9 306.4 2.0 590.3 3.6 149.3 0.9 277.9 1.7

8.5 8.6 13.4 12.2 38.4 35.1 16.4 15.7 76.6 7.4 19.7 19.5

Wet basis ratio was calculated dividing each adipose tissue concentration by each serum concentration (ng/mL); lipid basis ratio was calculated dividing each adipose tissue concentration (ng/g lipid) by each serum concentration (ng/g lipid).

The results of bivariate analyses between persistent organic pollutants and socio-demographic characteristics are shown in Table 5. No statistically significant association was found between sex, BMI, or residence and the concentrations of any organochlorine pesticide or PCB. A positive and statistically significant correlation was found between adipose tissue p,p0 -DDE concentrations and age (Spearman coefficient¼0.2, 95% Confidence Interval¼0.2–0.8) and between PCB 153 and age (Spearman coefficient¼0.3, 95% Confidence Interval¼0.0–0.5). Serum p,p-DDE concentrations were 6.5-fold higher in non-manual vs. manual workers, and serum PCB 180 concentrations were 2.7-fold higher in non-manual workers. These two associations were borderline statistically significant.

7.6 8.2 16.1 13.9 0.8 16.6 11.6 11.3 37.8 36.5 10.2 10.2

0.0 4.1 0.1 22.4 0.0 1.6 0.0 3.8 0.4 61.8 0.0 3.0

0.2 48.8 9.5 2185.8 0.5 143.1 1.0 214.5 2.9 517.2 0.6 123.6

5.9 5.8 5.7 5.6 1.6 1.5 1.8 1.7 2.3 2.2 2.3 2.1

19.3 24.1 92.9 116.1 1.3 1.7 61.6 77.0 2.7 33.5 6.8 8.5

55.5 69.4 889.1 1111.4 194.0 242.5 178.7 223.4 22.8 284.8 242.0 302.5

Table 4 Spearman correlation tests between concentrations of selected persistent organic pollutants. HCB Serum (ng/g lipid) HCB – p,p0 -DDE 0.2n p,p0 -DDT 0.1 PCB 138 0.2 PCB 153  0.4nn PCB 180 0.4n HCB

p,p0 -DDE

p,p0 -DDT

PCB 138

PCB 153

– – 0.1 0.2nn  0.0 0.1

– – – 0.2 0.2nn 0.4nn

– – – –  0.1 0.2

– – – – –  0.2

p,p0 -DDE

p,p0 -DDT

PCB 138

PCB 153

– – 0.3nn 0.6nn  0.1

– – – – 0.5nn 0.1

– – – – – 0.0

p,p0 -DDT

PCB 138

PCB 153

PCB 180

 0.2

0.0

0.1

 0.1

Adipose tissue (ng/g lipid) HCB – – p,p0 -DDE 0.2n – nn 0 p,p -DDT  0.2 0.2n PCB 138 0.0 0.1 PCB 153  0.1 0.1 PCB 180 0.2nn 0.2 HCB

3.3. Persistent organic pollutant concentrations and socio-demographic characteristics

75th

p,p0 -DDE

Adipose tissue vs. serum 0.2n 0.3nn

Adipose tissue vs. serum indicates correlations between adipose tissue and serum concentrations of each chemical. n

p o0.10. po 0.05.

nn

4. Discussion This is the first study of human exposure to persistent organic pollutants in Bolivia. Very little is known about current or past uses of organochlorine pesticides and PCBs in this country, and there are no previous records on human or environmental persistent organic pollutant levels in the study area. However, substantial levels of these compounds have been reported in

0.1) 0.1) 0.3) 0.1) 0.4) 0.2) to to to to to to (  0.3 (  0.2 (  0.3 (  0.3 (  0.1 (  0.1  0.1  0.1  0.1  0.1 0.2 0.1 (  0.3 to 0.3) (  0.2 to 0.2) (  0.3 to 0.2) (–0.4 to 0.1) (  0.2 to 0.2) (  0.3 to 0.3) 0.1  0.1  0.1 –0.2 0.1  0.1  0.1 (  0.3 to 0.2) 0.20 (  0.1 to 0.5)  0.1(  0.4 to 0.1) 0.01 (  0.3 to 0.3) 0.3 (0.0–0.5)  0.1 (  0.4 to 0.2) (4.3–80.4) (326.1–2797.4) (7.6–176.8) (6.6.253.1) (2.2–864.4) (35.9–224.1) 18.5 1119.4 36.63 40.8 43.9 55.90 (11.8–37.8) (84.9–345.7) (4.2–21.3) (15.0–53.2) (29.6–190.2) (10.6–38.3) 21.1 171.3 9.5 28.2 75.0 20.2 (4.7–36.8) (91.6–546.5) (1.1–40.9) (14.1–204.8) (3.2–292.9) (5.5–65.6) 13.2 376.5 6.6 53.7 30.6 19.0 (12.7–44.9) (97.2–446.8) (6.8–32.3) (12.6–47.7) (35.2–235.0) (13.5–51.7) 23.9 208.4 14.8 24.5 90.9 26.4 (12.3–40.6) (104.6–447.0) (6.3–26.6) (16.1–55.0) (27.2–176.2) (13.4–47.2) (4.5–96.4) (125.2–6636.4) (0.6–308.1) (4.5–1055.7) (0.5–1025.3) (4.6–318.5) 20.7 911.4 13.6 68.7 23.5 38.4

22.4 216.27 12.9 29.8 69.2 25.1

to to to to to to (  0.1 (  0.2 (  0.3 (  0.3 (  0.3 (  0.3 0.1 –0.02  0.1  0.1  0.1  0.1 (  0.2 to 0.2) (–0.1–0.3) (  0.3 to 0.1) (  0.3 to 0.2) (  0.3 to 0.2) (  0.2 to 0.2)  0.1 0.1  0.1  0.11  0.1 0.1 (  0.2 to 0.4) (0.2–0.8) (  0.3 to 0.2) (  0.3 to 0.3) (  0.3 to 0.2) (  0.4 to 0.1) 0.1 0.6  0.1 –0.1 0.1  0.1 (8.6–51.3) (177.3–698.0) (32.2–216.4) (41.0–232.0) (39.4–238.5) (15.5–109.3) 21.0 351.8 83.4 97.5 97.0 41.2 (18.5–36.7) (295.0–587.8) (16.9–55.6) (73.5–146.7) (34.4–95.8) (22.6–55.8) 26.1 416.4 30.7 103.9 57.4 35.5 (11.8–45.3) (161.2–515.8) (18.2–129.5) (54.1–200.9) (29.2–152.7) (14.5–74.9) 23.2 288.32 48.5 104.2 66.7 32.9 26.5(18.0–38.9) 476.1 (331.8–683.0) 37.3 (20.3–68.6) 107.7 (72.5–160.1) 66.6 (39.2–113.1) 42.1 (25.5–69.3) (17.5–32.7) (284.6–569.0) (23.1–74.2) (79.0–165.7) (41.1–111.2) (23.5–61.5) 25.5 402.4 41.4 114.4 67.6 38.0 (13.8–64.1) (135.2–809.3) (12.4–106.0) (33.4–165.2) (22.6–154.7) (20.2–155.2) 29.7 330.8 36.3 74.3 59.1 56.0

Adipose tissue HCB p,p0 -DDE p,p0 -DDT PCB 138 PCB 153 PCB 180 Serum HCB p,p0 -DDE p,p0 -DDT PCB 138 PCB 153 PCB 180

Spearman Spearman Spearman Non-manual Geometric mean (95%CI) Urban Geometric mean (95%CI) Woman Geometric mean (95%CI) Man Geometric mean (95%CI)

Rural Geometric mean (95%CI)

Manual Geometric mean (95%CI)

BMI Age Occupational categories Residence Sex

Table 5 Persistent organic pollutant concentrations and socio-demographic characteristics. Bivariate analysis.

0.2) 0.2) 0.1) 0.1) 0.1) 0.1)

J.P. Arrebola et al. / Environmental Research 112 (2012) 40–47

Cigarettes/week

44

environmental samples from surrounding regions (e.g., organochlorine pesticides in the air of the Andes Mountains in eastern Bolivia and DDT in river sediments in the southern Amazon region of Brazil), which could be potential sources of exposure via longrange atmospheric transport (Estellano et al., 2008; Torres et al., 2002; UNEP, 2002). Detectable levels of at least one persistent organic pollutant were found in the serum and adipose tissue of all study subjects, indicating that human exposure to these chemicals in Bolivia is widespread. In general, the detection frequencies of organochlorine pesticides and PCBs were similar to recent findings in various populations in South America, Europe, and Asia (Arrebola et al., 2009, 2010; Cerrillo et al., 2006; Munoz-de-Toro et al., 2006; Tan et al., 2008) with the exception of serum PCBs, whose detection was slightly less frequent than usually reported in more industrialized countries (CDC, 2009; Donato et al., 2008; Kang et al., 2008; Zubero et al., 2009). There have been no published human biomonitoring studies in Bolivia with which to compare our results. In general, the adipose tissue concentrations of p,p0 -DDE found in the present study (386.6 ng/g lipid) are in a similar magnitude to reports in countries that have banned the use of DDT for all purposes (Botella et al., 2004; Cerrillo et al., 2006; Hardell et al., 2006; Munoz-de-Toro et al., 2006; Tan et al., 2008). However, they are far lower than the concentrations of 2500 ng/g lipid found in Japan (Kunisue et al., 2007) and the 1.5 mg/kg described in India, where DDT remains in legal use for vector control (Aulakh et al., 2007). Waliszewski et al. (2010) reported adipose tissue organochlorine pesticide concentrations in two Mexican populations. One of these (Veracruz), with a known and extensive past use of DDT, had median p,p0 -DDE and p,p0 -DDT concentrations of 1829 and 114 ng/g lipid, respectively, while the other (Puebla), with a lesser reported use of DDT, showed very similar median concentrations to those in the present study (352 and 56 ng/g lipid, respectively). Additionally, serum concentrations of p,p0 -DDE (267.4 ng/g lipid) and p,p0 -DDT (13.0 ng/g lipid) in the present population were lower than findings in some areas where DDT remains in use for vector control (Rollin et al., 2009; Waliszewski et al., 2004) and similar to some reports in other regions of the world (Glynn et al., 2003; Kang et al., 2008; Karrman et al., 2006; Turci et al., 2010). Higher levels of these chemicals were reported in Spain by Jakszyn et al. (2009) and in New Zealand, Bates et al. (2004). HCB concentrations in adipose tissue and serum (26.3 and 22.1 ng/g lipid, respectively) were comparable to the majority of recent findings worldwide (Arrebola et al., 2009; Glynn et al., 2003; Hardell et al., 2006; Kang et al., 2008; Karrman et al., 2006; Munoz-de-Toro et al., 2006; Ociepa-Zawal et al., 2010; Waliszewski et al., 2010). There are no available records on the use of HCB in Bolivia (UNEP, 2002), but neighboring areas of Brazil are known to contain highly contaminated sites and stockpiles of HCB, which may be a significant environmental source (CETESB, 2011). PCBs have been reported to be one of the most important persistent toxic substances in South America, mostly derived from heavily industrialized and urbanized areas with high energy demand and disposal sites (UNEP, 2002). In the present study, the greatest contribution to total PCBs was PCB congener 153 in serum (59.0 ng/g lipid) and PCB 138 in adipose tissue (105.0 ng/g lipid). It has been proposed that congeners 138, 153, and 180 make the highest contribution to total adipose tissue PCBs in nonoccupationally exposed populations (Bergonzi et al., 2009; Covaci et al., 2008; Fernandez et al., 2008; Kiviranta et al., 2005; Wingfors et al., 2000). Serum and adipose tissue concentrations of PCBs were not very different from those reported in more industrialized

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countries (CDC, 2009; Covaci et al., 2008; Fernandez et al., 2008; Ibarluzea et al., 2011; Kalantzi et al., 2011; Kang et al., 2008; Thomas et al., 2006; Tsukino et al., 2006). This finding could be partly due to the rapid growth of the city of Santa Cruz de la Sierra over the past few decades, from 325,000 inhabitants in 1976 to 1,616,063 in 2009 (INE, 2010), involving a huge increase in both legal and illegal construction and industrial activities, which may have increased the recent contamination by PCBs in the local environment. No data are currently available on human exposure to PCBs in Bolivia. In our study population, both wet and lipid-adjusted persistent organic pollutant concentrations were higher in adipose tissue than in serum. Reported adipose tissue:serum ratios are usually between 50 and 200 in wet basis and around 1 in lipid basis, comparable to findings for most compounds in the present study. Lopez-Carrillo et al. (1999) found a similar ratio of lipid-basis concentrations for p,p0 -DDE (1.1) and a considerably lower wetbasis ratio (5.8) in one Mexican population, and Waliszewski et al. (2000) reported a slightly lower ratio of lipid-basis concentrations for p,p0 -DDE (0.9) and total DDT (0.8) in another, but a similar HCB ratio of lipid-basis concentrations (1.4) to the present finding. Mussalo-Rauhamaa (1991) found a similar ratio for p,p0 -DDE in both wet (330) and lipid basis (2.2) but a lower ratio for HCB in both wet (55) and lipid basis (0.2). Wet-basis ratios for persistent organic pollutants were reported to be 78.6–119.5 in an USA population (Stellman et al., 1998) and 66.4–199.3 in an Indian population (Rusiecki et al., 2005), who also showed lipid-adjusted adipose tissue:serum ratios o1 for PCBs 153 and 180. Positive and statistically significant correlations were observed between adipose tissue and serum concentrations of p,p0 -DDE and HCB but not of the remaining persistent organic pollutants, confirming reports that serum or plasma concentrations may not provide an accurate representation of concentrations in adipose tissue in all situations (Aronson et al., 2000). Reports on correlations between serum and adipose tissue concentrations range from negative values to coefficients above 0.8 (ArchibequeEngle et al., 1997; Aronson et al., 2000; Lopez-Carrillo et al., 1999; Mussalo-Rauhamaa, 1991; Rusiecki et al., 2005). Knowledge remains limited on relationships between serum and adipose tissue concentrations of persistent organic pollutants (Gaskins and Schisterman, 2009). Concentrations in the two matrixes have different biological meanings: adipose tissue levels have been proven to be a good indicator of cumulated long-term exposure, whereas serum levels are considered a measure of current exposure and the mobilization of persistent organic pollutants from fatty tissues (Archibeque-Engle et al., 1997; Crinnion, 2009). Limitations of our study include the relatively small size of the sample, which was also not entirely representative of the general population of Santa Cruz. However, this is the first study to characterize human exposure to these pollutants in a cohort living in Bolivia, and these data point to the urgent need for systematic human biomonitoring studies in South America, where persistent organic pollutants were banned relatively recently and there is evidence of their continued illegal use. A further study strength is that our data derive from two different biological matrices and yield useful information on both acute and chronic exposure. Santa Cruz de la Sierra, the setting of the present investigation, presents specific characteristics in terms of urban development that make it difficult to compare our results with findings in other populations. Bivariate analyses showed that sex, age, and BMI alone explained only a small proportion of the variability in persistent organic pollutant concentrations in the study population; hence, further possible confounders must be considered in

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future research. Consequently, specific modeling of each group of chemicals is required in order to assess the true predictors of the exposure. In this regard, our research group recently characterized the specific exposure predictors of p,p0 -DDT and p,p0 -DDE in the present cohort (Arrebola et al., 2012). Wider and more complex studies are warranted to elucidate the influence of anthropometric, socio-demographic, and dietary factors on the exposure of these populations.

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